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Original Research |
1 Department of Nuclear Medicine, New York University School of Medicine, New
York, NY 10016.
2 Department of Radiology, New York University School of Medicine, 550 First
Ave., New York, NY 10016.
3 Department of Orthopedic Surgery, New York University School of Medicine, New
York, NY 10016.
Received July 26, 2004;
accepted after revision October 20, 2004.
Address correspondence to E. L. Kramer
(elissa.kramer{at}msnyuhealth.org).
Abstract
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SUBJECTS AND METHODS. Twenty-four patients undergoing 18F-FDG PET for clinical oncologic assessment completed questionnaires regarding history of shoulder disease, trauma, pain, and/or functional impairment. Thorough physical examination of the shoulder was performed. A clinical diagnosis of specific shoulder derangement or normal was established for each patient. PET scans were evaluated blindly by a nuclear medicine physician and a musculoskeletal radiologist qualitatively for location, distribution, and intensity of shoulder uptake. Standardized uptake values (SUV) were measured.
RESULTS. Twenty-one patients had shoulder PET findings. Fourteen had clinical findings consistent with a specific diagnosis in the PET-positive shoulder. The remaining seven PET-positive patients were clinically normal. Three recognizable patterns of uptake were appreciable. Eight of 10 patients with diffuse uptake had findings of osteoarthritis (n = 7) or bursitis (n = 1). Two of four patients with focal greater tuberosity uptake had findings of rotator cuff injury. Two of four patients with focal glenoid uptake had findings of frozen shoulder. SUV showed a positive correlation with subject age (p < 0.01), but no association with clinical findings was identified.
CONCLUSION. The pattern of FDG uptake within the shoulder may point to specific clinical entities. While focal uptake is less reliably related to clinical findings, diffuse uptake is associated with signs and symptoms of osteoarthritis or bursitis.
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One study evaluated the significance of major joint uptake of FDG and found that the degree of uptake as measured by maximum standardized uptake value (SUV) correlated with age but not clinical symptomatology [4]. However, those authors examined only the intensity of joint uptake without evaluating the pattern or distribution of FDG accumulation within joints. We hypothesized that pattern and distribution of uptake may add to the understanding of the significance of FDG joint accumulation with regard to clinical disease.
Our study aimed to associate signs and symptoms of shoulder derangements with specific patterns of FDG uptake on PET. The shoulder joint was chosen as the focus of the study because shoulder pain is a common musculoskeletal complaint, with a prevalence of 7-20% in the adult population [5, 6], and the restricted movement associated with shoulder disease carries a high burden of disability.
We evaluated a series of patients for shoulder derangement using a combination of questionnaires and physical examination. These findings were viewed in the context of qualitative and semiquantitative PET analysis of the shoulder joint to determine if the pattern, distribution, and degree of PET uptake related to clinical derangement.
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FDG PET Scans
Total body PET scans were performed at the request of the referring
physician. Each subject was asked to fast for at least 6 hr. Blood glucose
levels were lower than 150 mg/dL in all subjects. Forty-five minutes after an
IV injection of 10-15 mCi (370-550 MBq) 18F-FDG, imaging was
performed with an Advance PET System (GE Healthcare). Patients were asked to
recline quietly without moving their arms during the uptake period. Patients
were positioned for the scan with arms down in a neutral (thumbs up) position
and whole-body scans from the skull to midthigh were acquired using a 2D
protocol with 5 min emission and 3 min transmission per bed position. Images
were reconstructed using an iterative reconstruction algorithm and attenuation
correction.
PET images were analyzed jointly by a nuclear medicine physician and a musculoskeletal radiologist, both of whom were blinded to the history and physical examination findings. Scans were initially evaluated to ensure absence of metastatic disease in the area of the shoulder and compliance with exclusion criteria. Two subjects were noted to have significant uptake in the muscles of the upper arm secondary to arm motion during the radiotracer uptake period. This limited the accuracy of shoulder reading and both subjects were excluded from the study. The remaining 24 scans were evaluated qualitatively for location, distribution, and relative intensity of shoulder uptake. In addition, semiquantitative measurements of SUV were taken using regions of interest (ROIs) over the entire shoulder. These SUVs were calculated using the formula: SUV = (decay-corrected measured activity [mCi/g] / (administered dose [mCi]) / patient weight [g]). The ROIs encompassed the humeral head, glenohumeral joint, and acromioclavicular (AC) joint. The maximum and mean SUVs within that ROI were recorded in the 8-10 coronal slices that included the shoulder joint.
Clinical Assessment
After the scan, participants completed a questionnaire created by the
investigators to assess the presence and severity of shoulder disease. Using a
yes/no format, the questionnaire inquired specifically about history of
injury, arthritis, frozen shoulder, and/or use of analgesics related to
shoulder pain. A "yes" response to any question required
completion of an area of free text to provide further detail, including time
of diagnosis and treatment. The questionnaire also provided an opportunity for
participants to describe joint problems elsewhere in the body. The handedness
of the patients was not ascertained.
Subjects also completed the Disabilities of the Arm, Shoulder, and Hand (DASH) questionnaire [7, 8]. This questionnaire evaluates impairments in activities of daily living secondary to symptoms of the upper extremity. The DASH questionnaire consists of 30 statements to which the participant provided a numeric score of agreement (1-5). A DASH score (scale 0-100) was calculated for each participant according to the formula included with the questionnaire.
The physical examination of the shoulder was performed by a third-year medical student who had been trained by an experienced orthopedic surgeon. The focused physical examination of the shoulder consisted of visual inspection of the arms, shoulders, neck, and back for symmetry, atrophy, and gross defects. Both active and passive assessments were made of the range of motion of the shoulder joint about all axes. Flexion, extension, internal rotation, external rotation, abduction, adduction, and horizontal adduction were measured using a goniometer. The anterior apprehension test, posterior apprehension test, and sulcus sign were performed to elicit evidence of instability of the glenohumeral joint in the anterior, posterior, and inferior directions, respectively. The general integrity of the rotator cuff muscles was evaluated with the drop sign, the strength of the supraspinatus with the empty can test, and the strength of the subscapularis with the lift-off test. In addition, attempts at eliciting the Hawkins sign and Neer classification were made to evaluate the possibility of impingement of structures within the subacromial space. The data from the history and physical examinations were reviewed by an orthopedic surgeon. Where possible, a diagnosis was established for each patient with clinical pathology, based on the questionnaires and physical examination. Patients without any history of shoulder disease and/or without clinical derangement were considered normal. In addition, patients at or under 51 years old with small limitations in range of motion isolated to one axis were also considered normal.
Results of CT or MRI of the shoulders were not consistently available in these subjects for comparison. Furthermore, PET was performed with the arms in a neutral position because these patients were being evaluated for their cancers. The CT scans that were available to us were consistently performed with the patients' arms raised over their heads making direct comparison difficult. At times, the field of view on the CT image excluded the shoulder. Specific anatomic imaging of the shoulder was not performed in the patients for this study nor was it available for evaluation.
Statistical Analysis
The clinically negative and clinically positive patients were compared with
respect to primary DASH score and maximum SUV using the Wilcoxon's rank sum
test. Logistic regression was conducted to examine the utility of the primary
DASH score and maximum SUV as indicators of clinical status (clinically
positive vs clinically negative) after adjusting for the potential confounding
effects of age and sex. The associations among age, primary DASH score, and
maximum SUV were assessed through Spearman's rank and Pearson's product moment
correlation coefficients. All statistical tests were conducted at the
two-sided 5% significance level and all p values reported are
correspondingly two-sided.
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With regard to PET results, 14 patients had both history and physical findings consistent with a specific diagnosis and PET findings. Five patients had positive PET findings but no history of shoulder disease and no evidence of shoulder derangements on physical examination. Three patients had no PET findings and negative histories and physicals. Two patients had abnormal uptake but clinical findings in contralateral shoulders.
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Four subjects had PET findings of asymmetric localized uptake at the greater tuberosity (Table 2). Two of these patients had known rotator cuff injuries. Physical examination revealed predominant subscapularis disease in one patient and more clinically generalized rotator cuff disease in the other. One of the remaining subjects had a diagnosis of frozen shoulder and a principal PET finding of asymmetric glenoid uptake in that shoulder. The final patient with focal greater tuberosity uptake was asymptomatic.
The pattern of focal glenoid uptake was seen in four subjects (Table 2). Two of these subjects had a history of frozen shoulder and physical examination findings consistent with this diagnosis, one of whom also had a secondary finding of asymmetric glenoid uptake. The third patient with focal glenoid uptake had a history and physical examination that pointed to a diagnosis of osteoarthritis. This patient not only had focal glenoid uptake but also circumferential/diffuse uptake. The final subject had glenoid uptake in a clinically negative shoulder.
In the remaining two clinically and PET-positive patients, correlation with clinical diagnoses was less consistent. Focal asymmetric AC uptake and a clinically significant limitation in range of motion were noted in a subject with massive lymphedema after surgical resection of axillary lymph nodes for breast cancer. A similar pattern of uptake was noted in the contralateral arm of one of the previously accounted for patients with rotator cuff injury and greater tuberosity uptake. This patient had congenital Erb's palsy and also presented with a severely limited range of motion secondary to this abnormality. A third patient with AC uptake was asymptomatic. The final clinically and PET-positive patient had a history of anterior shoulder instability bilaterally with a recent right-sided dislocation and was noted to have an accumulation of FDG in the region of the subscapularis bursa.
In the seven patients with abnormal PET uptake and no signs and symptoms of shoulder disease, four patterns of uptake were noted: capsular outline, patchy accumulation over the glenohumeral area, focal uptake at the surgical neck of the humerus, and focal coracoid uptake. This raises the possibility that these findings are not disease related or represent subclinical disease.
Statistical Analyses
Analyses of SUVs were performed to identify quantitative differences in FDG
uptake. When comparing patients with and without clinical symptoms, no
statistically significant variation in maximum SUV was appreciated
(Wilcoxon's, p = 0.806; logistic, p = 0.767). Furthermore,
the maximum SUV among the 14 patients with both clinical and PET findings
compared with the three clinically and PET-negative patients showed no
statistically significant difference (Wilcoxon's, p = 0.899;
logistic, p = 0.832) (Table
3). However, the maximum SUV did exhibit a statistically
significant positive correlation (p < 0.01) with age, increasing
an average of 0.023 units for each 1 year increase in subject age as noted by
others [4]
(Fig. 4). Pearson's and
Spearman's correlations revealed no significant association of DASH score with
either maximum SUV or age.
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We used clinical assessment as our gold standard for comparison with FDG PET findings. The core component of this study involved careful examination of the shoulder joint, including assessment of range of motion and specific maneuvers to elicit signs of shoulder disease. All physical examination techniques used in this study are well established and produce reliable results. For example, the Hawkins sign has demonstrated a sensitivity of 88% and 92% for cuff abnormalities and bursitis, respectively [13]. Like-wise, the lift-off sign has been shown to have a positive predictive value of 100% and a negative predictive value of 69% for subscapularis abnormality [14]. Thus, the information derived from the examination, when taken in the context of a full history, should provide significant opportunity for an accurate clinical diagnosis of acute derangements.
However, in patients with long-standing shoulder disease, the sensitivities and specificities of physical examination maneuvers may be decreased and clinical assessment becomes more difficult [15]. Thus, clinical diagnosis may be less accurate in this setting. In addition, the presence of multiple derangements in a given shoulder may complicate clinical evaluation even further. For instance, one subject had circumferential/diffuse uptake and a focus of uptake at the greater tuberosity, consistent with osteoarthritis and rotator cuff disease, respectively. While the physical examination revealed rotator cuff injury, this finding may have overshadowed an element of osteoarthritis. This patient underscores the types of difficulties that can be encountered when interpreting clinical data.
In rotator cuff disease, inflammatory changes would be expected with acute injury. In this study, both patients with a history of rotator cuff tear and a PET finding of focal greater tuberosity uptake had suffered their initial injury several years prior but remained symptomatic. Whether any degree of chronic inflammation may remain in the soft tissues for a prolonged period of time after a rotator cuff tear remains unclear. The location of the uptake observed in these patients, however, is consistent with the anatomy of the rotator cuff. The greater tuberosity is the site of insertion of the supraspinatus, which may be affected in the patient with generalized rotator cuff disease. The second patient had predominantly subscapularis involvement, which would be expected to produce uptake where the muscle inserts at the lesser tuberosity. This discrepancy may be a manifestation of the relatively poor anatomic resolution of PET alone because the greater and lesser tuberosities are closely related. PET/CT might help to better elucidate this point.
Frozen shoulder is an orthopedic entity for which the exact cause and pathophysiology are poorly understood. Trauma, surgery, diabetes, and inflammatory diseases have all been linked to the condition [16]. Frozen shoulder may have a local inflammatory component in the shoulder, but not enough is known about this disease to fully understand what, if any, the significance of coracoid uptake may be.
While the remaining patterns of FDG accumulation appeared less consistently with specific diseases of the shoulder, one theory emerged about focal AC uptake. Two of the three patients with this finding had conditions outside of the shoulder that limit normal functioning of the joint: one patient had massive lymphedema after axillary lymph node resection for breast cancer and the other had congenital Erb's palsy. These patients might compensate for their disability by overusing the shoulder and stressing the AC joint. This mechanism might account for the local FDG uptake in that area.
Overall, it seems that PET has a high sensitivity for detecting joint derangement because only two patients in this series had clinical shoulder derangement in the absence of abnormal FDG uptake. One previous study comparing PET to MRI for quantification of inflammation within the wrists of patients with inflammatory arthritides found that FDG and gadolinium uptake were closely correlated with each other and were also associated with clinical findings [17]. This suggests that the sensitivity of PET may be similar to that of MRI, at least for some joint diseases. The specificity of PET, however, might be somewhat lower. False-positive PET findings occurred with some frequency in this study, particularly for diagnoses of rotator cuff disease and frozen shoulder. Determining the specificity of FDG accumulation requires further evaluation in a larger number of subjects and, perhaps, with a more sensitive gold standard than clinical evaluation.
Currently, MRI is the accepted imaging tool for evaluating the shoulder. Its anatomic resolution allows for visualization of not only the bone components of the shoulder but also the soft tissues of the joint, including the rotator cuff muscles, labral-capsular complex, and subacromial/subdeltoid bursae. The diagnostic value of MRI is greatest in the assessment of full-thickness rotator cuff tears, for which it has a sensitivity of 81% [18, 19] and is considered comparable in accuracy to sonography [18] and arthrography [19]. However, MRI is less sensitive for partial rotator cuff tears and other abnormal conditions of the shoulder including labral tears [20]. A newer application involves dynamic MRI with contrast enhancement, which is capable of demonstrating inflammatory changes of synovial tissue in subacromial bursitis [21], rheumatoid arthritis [22], and osteoarthritis [22]. Because inflammatory lesions have a high rate of glucose metabolism, they also may be amenable to evaluation by FDG PET.
From this study, it is clear that shoulder uptake is a common finding on PET. While FDG accumulates in varying intensities, likely as a manifestation of age, the pattern and distribution of FDG may point to specific clinical diseases of the shoulder. In particular, circumferential/diffuse uptake of FDG seems to be associated with osteoarthritis. Despite the small sample size, this study suggests that focal greater tuberosity and glenoid uptake may be related to rotator cuff disease and frozen shoulder, respectively. However, correlating PET findings with MRI may be required for fully evaluating FDG uptake within the shoulder and determining the clinical role of FDG PET for assessing inflammatory activity in shoulder derangements. Results from a larger series with correlation using MRI or surgically proven cases may be necessary before we can use FDG PET to definitively diagnose shoulder abnormalities. Nonetheless, the recognition of these patterns of uptake in association with musculoskeletal disease of the shoulder may help explain shoulder pain in the cancer patient.
Acknowledgments
We thank Victor Moran for the time and technical expertise he contributed
to this project.
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